Skip to main content

Genomic relationships between hexaploid Helianthus resinosus and diploid Helianthus annuus (Asteraceae)

Abstract

Genus Helianthus comprises diploid and polyploid species. An autoallopolyploid origin has been proposed for hexaploid species but the genomic relationships remain unclear. Mitotic and meiotic studies in annual Helianthus annuus (2n = 2x = 34) and perennial Helianthus resinosus (2n = 6x = 102) as well as the F1 hybrids between both species were carried out. Chromosome counting confirmed the hybrid origin of the latter plants and their tetraploid condition. Bivalents in hybrids ranged from 12 to 28 (\( \bar{x} \) = 20.8). Univalents, trivalents and quadrivalents were also observed. Meiotic products comprised dyads, triads and normal tetrads and pollen grains were heterogeneous in size. These observations suggest the occurrence of 2n pollen in addition to the expected n. Genomic in situ hybridization (GISH) of total H. annuus DNA on H. resinosus chromosomes rendered weak but uniform signals; similar hybridization pattern was observed using three other annual species. Hybridization with H. annuus probe performed on root tip cells of F1 H. annuus × H. resinosus hybrids revealed 17 chromosomes with a strong hybridization signal. GISH in hybrid meiocytes distinguished chromosomes from parental species and revealed autosyndetic pairing of H. resinosus chromosomes, allosyndetic pairing in bivalents, trivalents and quadrivalents, and the presence of univalents derived from parents, H. annuus and H. resinosus. Results obtained from classical and molecular cytogenetics do not support H. annuus as a direct ancestor of H. resinosus. The occurrence of allosyndetic pairing and the relatively high fertility of the F1 hybrids point to the possibility that useful genes could be transferred from H. resinosus to cultivate sunflower, although the effective rate of recombination has not been evaluated. GISH method proved effective to recognize parental chromosomes in H. annuus × H. resinosus progeny.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

CTAB:

Cetyltrimethylammonium bromide

ETS:

External Transcribed Spacer

FISH:

Fluorescence in situ hybridization

GISH:

Genomic in situ hybridization

ITS:

Internal Transcribed Spacer

References

  • Atlagic J (1996) Cytogenetic studies in hexaploid Helianthus species and their F1 hybrids with cultivated sunflower, H. annuus. Plant Breed 115:257–260

    Article  Google Scholar 

  • Atlagic J, Dozet B, Skoric D (1995) Meiosis and pollen grain viability in Helianthus mollis, Helianthus salicifolius, Helianthus maximiliani and their F1 hybrids with cultivated sunflower. Euphytica 81:259–263

    Article  Google Scholar 

  • Bennett ST, Kenton AY, Bennett MD (1992) Genomic in situ hybridization reveals the allopolyploid nature of Milium montianum (Gramineae). Chromosoma 101:420–424

    Article  Google Scholar 

  • Camadro EL, Saffarano SK, Espinillo JC, Castro M, Simon PW (2008) Cytological mechanisms of 2n pollen formation in the wild potato Solanum okadae and pollen-pistil relations with the cultivated potato, Solanum tuberosum. Genet Resour Crop Ev 55:471–477

    Article  Google Scholar 

  • Carrera A, Poverene M, Rodriguez R (2004) Isozyme and cytogenetic analysis in Helianthus resinosus Small. Proc Intern Sunflower Conf. Vol II, Fargo, pp 685–691

    Google Scholar 

  • Cavallini A, Natali L, Zuccolo A, Giordani T, Jurman I, Ferrillo V, Vitacolonna N, Sarri V, Cattonaro F, Ceccarelli M, Cionini PG, Morgante M (2010) Analysis of transposons and repeat composition of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 120:491–508

    CAS  PubMed  Article  Google Scholar 

  • Ceccarelli M, Sarri V, Natali L et al (2007) Characterization of the chromosome complement of Helianthus annuus by in situ hybridization of a tandemly repeated DNA sequence. Genome 50:429–434

    CAS  PubMed  Article  Google Scholar 

  • Chandler JM (1991) Chromosome evolution in sunflower. In: Tsuchiya P, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution. Part B. Elsevier, Amsterdam, pp 229–249

    Google Scholar 

  • Chester M, Leitch AR, Soltis PS, Soltis DE (2010) Review of the application of modern cytogenetic methods (FISH/GISH) to the study of reticulation (polyploidy/hybridization). Genes 1:166–192

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • CIMMYT (2005) Laboratory Protocols: CIMMYT Applied Molecular Genetics Laboratory, 3rd edn. CIMMYT, Mexico, DF

  • Cuellar T, Belhassen E, Fernandez-Calvin B, Orellana J, Bella JL (1996) Chromosomal differentiation in Helianthus annuus var macrocarpus: heterochromatin characterization and rDNA location. Heredity 76:586–591

    Article  Google Scholar 

  • Echeverría MM, Salaberry MT, Rodríguez RH (2003) Characterization for agronomic use of cytoplasmic male-sterility in sunflower (Helianthus annuus L.) introduced from H. resinosus small. Plant Breed 122:357–361

    Article  Google Scholar 

  • Espinasse A, Foueillassarl J, Kimber G (1995) Cytogenetical analysis of hybrids between sunflower and four wild relatives. Euphytica 82:65–72

    Article  Google Scholar 

  • Feng J, Liu Z, Cai X, Jan Ch (2013) Toward a molecular cytogenetic map for cultivated sunflower (Helianthus annuus L.) by landed BAC/BIBAC clones. G3 (Bethesda) 3(1):31–40. doi:10.1534/g3.112.004846

    CAS  Article  Google Scholar 

  • Fernandez P, Paniego N, Lew S, Hopp HE, Heinz RA (2003) Differential representation of sunflower ESTs in enriched organ-specific cDNA libraries in a small scale sequencing project. BMC Genomics 4:40. doi:10.1186/1471-2164-4-40

    PubMed Central  PubMed  Article  Google Scholar 

  • Garayalde A, Poverene M, Cantamutto M, Carrera A (2011) Wild sunflower diversity in Argentina revealed by ISSR and SSR markers: an approach for conservation and breeding programmes. Ann Appl Biol 158:305–317

    CAS  Article  Google Scholar 

  • Giordani T, Natali L, Cavallini A (2003) Analysis of a dehydrin encoding gene and its phylogenetic utility in Helianthus. Theor Appl Genet 107:316–325

    CAS  PubMed  Article  Google Scholar 

  • Heiser CB, Smith DM, Clevenger S, Martin WC (1969) The North American sunflowers (Helianthus). Mem Torrey Bot Club 22:1–218

    Google Scholar 

  • Humphreys MW, Thomas HM, Morgan WG, Meredith MR, Harper JA, Thomas H, Zwierzykowski A, Ghesquiere M (1995) Discriminating the ancestral progenitors of hexaploid Festuca arundinacea using genomic in situ hybridization. Heredity 75:171–174

    Article  Google Scholar 

  • Jan CC, Seiler GJ (2007) Sunflower. In: Singh RJ (ed) Genetics Resources, Chromosome Engineering, and Crop Improvement, vol 4., Oilseed CropsCRC Press, Taylor and Francis Group, New York, pp 103–165

    Google Scholar 

  • Kostoff D (1939) Autosynthesis and structure hybridity F1-hybrid H. tuberosus × H. annuus L. and their sequences. Genetica 21:285–300

    Article  Google Scholar 

  • Lim KY, Kovarik A, Matyasek R, Chase MW, Clarkson JJ, Grandbastien MA, Leitch AR (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756–763

    CAS  PubMed  Article  Google Scholar 

  • Liu Z, Feng J, Jan CC (2009) Genomic in situ hybridization (GISH) as a tool to identify chromosomes of parental species in sunflower interspecific hybrids. Proc Nat Sunflower Assoc ARS USDA. http://hdl.handle.net/10113/34842

  • Liu Z, Cai X, Seiler GJ, Gulya TA, Rashid KY, Jan CC. 2013. Update on transferring Sclerotinia resistance genes from wild perennial Helianthus species into cultivated sunflower. National Sclerotinia Initiative 2013 Annual Meeting. http://www.ars.usda.gov/SP2UserFiles/ad_hoc/54000000WhiteMoldResearch/2013Meeting/2013%20National%20Sclerotinia%20Initiative%20Annual%20Meeting.pdf

  • Mok DWS, Peloquin SJ (1972) Three mechanisms of 2n pollen formation in diploid potatoes. Am Potato J 49:362–363

    Google Scholar 

  • Mondolot-Cosson L, Andary C (1994) Resistance factors of a wild species of sunflower, Helianthus resinosus, to Sclerotinia sclerotiorum. Acta Hort (ISHS) 381:642–645

    CAS  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    CAS  PubMed  Article  Google Scholar 

  • Poggio L, Confalonieri V, Comas C, Cuadrado A, Jouve N, Naranjo CA (1999) Genomic in situ hybridization (GISH) of Tripsacum dactyloides and Zea mays ssp mays with B chromosomes. Genome 42:687–691

    CAS  Article  Google Scholar 

  • Prabakaran AJ, Sujatha M (2004) Interspecific hybrid of Helianthus annuus × H. simulans: characterization and utilization in improvement of cultivated sunflower (H. annuus L.). Euphytica 135:275–282

    CAS  Article  Google Scholar 

  • Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement —A review. Euphytica 133:3–18

    Article  Google Scholar 

  • Rieseberg LH (1991) Homoploid reticulate evolution in Helianthus (Asteraceae): evidence from ribosomal genes. Am J Bot 78:1218–1237

    Article  Google Scholar 

  • Rogers CE, Thompson TE, Seiler GJ (1982) Sunflower species of the United States. National Sunflower Association, Fargo

    Google Scholar 

  • Sala CA, Echarte AM (1996) Cytological mechanism of 2n pollen formation in interspecific polyploid hybrids of Helianthus. In: International Sunflower Association (ed) 14th Intern Sunflower Conf, pp 73

  • Schilling EE (1997) Phylogenetic analysis of Helianthus (Asteraceae) based on chloroplast DNA restriction site data. Theor Appl Genet 94:925–933

    CAS  Article  Google Scholar 

  • Schilling EE, Heiser CB (1981) Infrageneric classification of Helianthus (Compositae). Taxon 30:393–403

    Article  Google Scholar 

  • Schilling EE, Linder CR, Noyes RD, Rieseberg LH (1998) Phylogenetic relationships in Helianthus (Asteraceae) based on nuclear ribosomal DNA internal transcribed spacer region sequence data. Sys Bot 23:177–187

    Article  Google Scholar 

  • Sossey-Alaoui K, Serieys H, Tersac M, Lambert P, Schilling E, Griveau Y, Kaan F, Berville A (1998) Evidence for several genomes in Helianthus. Theor Appl Genet 97:422–430

    CAS  Article  Google Scholar 

  • Staton SE, Bakken BH, Blackman BK, Chapman MA, Kane NC, Tang S, Ungerer MC, Knapp SJ, Rieseberg LH, Burke JM (2012) The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements. Plant J 72:142–153

    CAS  PubMed  Article  Google Scholar 

  • Sujatha M, Prabakaran AJ (2006) Ploidy manipulation and introgression of resistance to Alternaria helianthi from wild hexaploid Helianthus species to cultivated sunflower (H. annuus L.) aided by anther culture. Euphytica 152:201–215

    Article  Google Scholar 

  • Talia P, Greizerstein E, Díaz Quijano C et al (2010) Cytological characterization of sunflower by in situ hybridization using homologous rDNA sequences and a BAC clone containing highly represented repetitive. Genome 53:1–8

    Article  Google Scholar 

  • Taschetto OM, Pagliarini MS (2003) Occurrence of 2n and jumbo pollen in the Brazilian ginseng (Pfaffia glomerata and P. tuberosa). Euphytica 133:139–145

    Article  Google Scholar 

  • Thompson TE, Zimmerman DC, Rogers CE (1981) Wild Helianthus as a genetic resource. Field Crop Res 4:333–343

    Article  Google Scholar 

  • Timme RE, Simpson BB, Linder CR (2007) High-resolution phylogeny for Helianthus (Asteraceae) using the 18S-26S ribosomal DNA external transcribed spacer. Am J Bot 94:1837–1852

    CAS  PubMed  Article  Google Scholar 

  • Veilleux R (1985) Diploid and polyploid gametes in crop plants: mechanisms of formation and utilization in plant breeding. Plant Breed Rev 3:253–288

    Google Scholar 

  • Vukich M, Schulman AH, Giordani T, Natali L, Kalendar R, Cavallini (2009) Genetic variability in sunflower (Helianthus annuus L.) and in the Helianthus genus as assessed by retrotransposon-based molecular markers. Theor Appl Genet 119:1027–1038

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We are grateful to MSc. Raúl Rodríguez for his knowledge and help in getting the plant material. This research was supported by Grants ANPCYT-PICT 2286 and UNS-PGI 24A160.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julieta Miranda Zanetti.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Miranda Zanetti, J., Greizerstein, E., Camadro, E. et al. Genomic relationships between hexaploid Helianthus resinosus and diploid Helianthus annuus (Asteraceae). Plant Syst Evol 300, 1071–1078 (2014). https://doi.org/10.1007/s00606-013-0945-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-013-0945-0

Keywords

  • 2n pollen
  • Allosyndesis
  • GISH
  • Interspecific hybrid
  • Polyploidy
  • Sunflower